Altered activation patterns by triceps surae stretch reflex pathways in acute and chronic spinal cord injury

Journal of Neurophysiology

Volumn 106, Issue 4, 2011, Pages 1669-1678

  Frigon, Alain ^a   Johnson, Michael D ^b   Heckman, C J ^b  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Force; Functional recovery; Muscle length

Indexed keywords

CLONIDINE;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC DISEASE; ELECTROMYOGRAPHY; EVOKED RESPONSE; GASTROCNEMIUS MUSCLE; LAMINECTOMY; MUSCLE CONTRACTION; MUSCLE SPINDLE; MYOTATIC REFLEX; NONHUMAN; PRIORITY JOURNAL; SEMITENDINOUS MUSCLE; SOLEUS MUSCLE; SPINAL CORD INJURY; TRICEPS SURAE MUSCLE;

ACUTE DISEASE; ANIMALS; BIOMECHANICS; CATS; CHRONIC DISEASE; CORDOTOMY; DECEREBRATE STATE; ELECTROMYOGRAPHY; REFLEX, STRETCH; SPINAL CORD INJURIES;

EID: 80054027954     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00504.2011     Document Type: Article

References (59)

1. Ahlman H, Grillner S, Udo M. The effect of 5-HTP on the static fusimotor activity and the tonic stretch reflex of an extensor muscle. Brain Res 27: 393-396, 1971.
2. Bailey CS, Lieberman JS, Kitchell RL. Response of muscle spindle primary endings to static stretch in acute and chronic spinal cats. Am J Vet Res 41: 2030-2036, 1980.
3. Belanger M, Drew T, Provencher J, Rossignol S. A comparison of treadmill locomotion in adult cats before and after spinal transection. J Neurophysiol 76: 471-491, 1996.
4. Bennett DJ, De Serres SJ, Stein RB. Gain of the triceps surae stretch reflex in decerebrate and spinal cats during postural and locomotor activities. J Physiol 496: 837-850, 1996.
5. Boulenguez P, Liabeuf S, Bos R, Bras H, Jean-Xavier C, Brocard C, Stil A, Darbon P, Cattaert D, Delpire E, Marsala M, Vinay L. Downregulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16: 302-307, 2010.
6. Bouyer LJ, Whelan PJ, Pearson KG, Rossignol S. Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy. J Neurosci 21: 3531-3541, 2001.
7. Burke D, Gandevia SC, McKeon B. Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 52: 435-448, 1984.
8. Burke D, Knowles L, Andrews C, Ashby P. Spasticity, decerebrate rigidity and the clasp-knife phenomenon: an experimental study in the cat. Brain 95: 31-48, 1972.
9. Cleland CL, Hayward L, Rymer WZ. Neural mechanisms underlying the clasp-knife reflex in the cat. II. Stretch-sensitive muscular-free nerve endings. J Neurophysiol 64: 1319-1330, 1990.
10. Cleland CL, Rymer WZ. Neural mechanisms underlying the clasp-knife reflex in the cat. I. Characteristics of the reflex. J Neurophysiol 64: 1303-1318, 1990.
11. Conway BA, Hultborn H, Kiehn O. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res 68: 643-656, 1987.
12. Cote MP, Gossard JP. Step training-dependent plasticity in spinal cutaneous pathways. J Neurosci 24: 11317-11327, 2004.
13. Cote MP, Menard A, Gossard JP. Spinal cats on the treadmill: changes in load pathways. J Neurosci 23: 2789-2796, 2003.
14. Cotel F, Antri M, Barthe JY, Orsal D. Identified ankle extensor and flexor motoneurons display different firing profiles in the neonatal rat. J Neurosci 29: 2748-2753, 2009.
15. Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB. Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126: 495-507, 2003.
16. Dietz V, Grillner S, Trepp A, Hubli M, Bolliger M. Changes in spinal reflex and locomotor activity after a complete spinal cord injury: a common mechanism? Brain 132: 2196-2205, 2009.
17. Ellaway PH, Trott JR. The mode of action of 5-hydroxytryptophan in facilitating a stretch reflex in the spinal cat. Exp Brain Res 22: 145-162, 1975.
18. Enriquez-Denton M, Morita H, Christensen LO, Petersen N, Sinkjaer T, Nielsen JB. Interaction between peripheral afferent activity and presynaptic inhibition of Ia afferents in the cat. J Neurophysiol 88: 1664-1674, 2002.
19. Frigon A, Barriere G, Leblond H, Rossignol S. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat. J Neurophysiol 102: 2667-2680, 2009.
20. Frigon A, Gossard JP. Evidence for specialized rhythm-generating mechanisms in the adult mammalian spinal cord. J Neurosci 30: 7061-7071, 2010.
21. Frigon A, Rossignol S. Adaptive changes of the locomotor pattern and cutaneous reflexes during locomotion studied in the same cats before and after spinalization. J Physiol 586: 2927-2945, 2008.
22. Frigon A, Rossignol S. Functional plasticity following spinal cord lesions. Prog Brain Res 157: 231-260, 2006.
23. Frigon A, Rossignol S. Plasticity of reflexes from the foot during locomotion after denervating ankle extensors in intact cats. J Neurophysiol 98: 2122-2132, 2007.
24. Granit R. Reflex self-regulation of muscle contraction and autogenetic inhibition. J Neurophysiol 13: 351-372, 1950.
25. Grey MJ, Ladouceur M, Andersen JB, Nielsen JB, Sinkjaer T. Group II muscle afferents probably contribute to the medium latency soleus stretch reflex during walking in humans. J Physiol 534: 925-933, 2001.
26. Guertin P, Angel MJ, Perreault MC, McCrea DA. Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol 487: 197-209, 1995.
27. Heckman CJ, Hyngstrom AS, Johnson MD. Active properties of motoneurone dendrites: diffuse descending neuromodulation, focused local inhibition. J Physiol 586: 1225-1231, 2008.
28. Hiersemenzel LP, Curt A, Dietz V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 54: 1574-1582, 2000.
29. Hochman S, McCrea DA. Effects of chronic spinalization on ankle extensor motoneurons. I. Composite monosynaptic Ia EPSPs in four motoneuron pools. J Neurophysiol 71: 1452-1467, 1994.
30. Holmqvist B, Lundberg A. Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol Scand Suppl 186: 1-15, 1961.
31. Ichiyama RM, Broman J, Roy RR, Zhong H, Edgerton VR, Havton LA. Locomotor training maintains normal inhibitory influence on both alphaand gamma-motoneurons after neonatal spinal cord transection. J Neurosci 31: 26-33, 2011.
32. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38: 335-378, 1992.
33. Jankowska E, Hammar I. Spinal interneurones; how can studies in animals contribute to the understanding of spinal interneuronal systems in man? Brain Res Brain Res Rev 40: 19-28, 2002.
34. Johnson MD, Heckman CJ. Interactions between focused synaptic inputs and diffuse neuromodulation in the spinal cord. Ann NY Acad Sci 1198: 35-41, 2010.
35. Leis AA, Kronenberg MF, Stetkarova I, Paske WC, Stokic DS. Spinal motoneuron excitability after acute spinal cord injury in humans. Neurology 47: 231-237, 1996.
36. Lundberg A, Malmgren K, Schomburg ED. Reflex pathways from group II muscle afferents. 1. Distribution and linkage of reflex actions to alphamotoneurones. Exp Brain Res 65: 271-281, 1987.
37. Mense S, Meyer H. Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J Physiol 363: 403-417, 1985.
38. Miller JF, Paul KD, Lee RH, Rymer WZ, Heckman CJ. Restoration of extensor excitability in the acute spinal cat by the 5-HT2 agonist DOI. J Neurophysiol 75: 620-628, 1996.
39. Mirbagheri MM, Barbeau H, Ladouceur M, Kearney RE. Intrinsic and reflex stiffness in normal and spastic, spinal cord injured subjects. Exp Brain Res 141: 446-459, 2001.
40. Morita H, Petersen N, Christensen LO, Sinkjaer T, Nielsen J. Sensitivity of H-reflexes and stretch reflexes to presynaptic inhibition in humans. J Neurophysiol 80: 610-620, 1998.
41. Musienko PE, Zelenin PV, Orlovsky GN, Deliagina TG. Facilitation of postural limb reflexes with epidural stimulation in spinal rabbits. J Neurophysiol 103: 1080-1092, 2010.
42. Nelson SG, Collatos TC, Niechaj A, Mendell LM. Immediate increase in Ia-motoneuron synaptic transmission caudal to spinal cord transection. J Neurophysiol 42: 655-664, 1979.
43. Nelson SG, Mendell LM. Enhancement in Ia-motoneuron synaptic transmission caudal to chronic spinal cord transection. J Neurophysiol 42: 642-654, 1979.
44. Nichols TR, Cope TC. The organization of distributed proprioceptive feedback in the chronic spinal cat. In: Motor Neurobiology of the Spinal Cord, edited by Cope TC. Boca Raton, FL: CRC, 2001.
45. Pearson KG, Fouad K, Misiaszek JE. Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. J Neurophysiol 82: 370-381, 1999.
46. Pearson KG, Misiaszek JE, Hulliger M. Chemical ablation of sensory afferents in the walking system of the cat abolishes the capacity for functional recovery after peripheral nerve lesions. Exp Brain Res 150: 50-60, 2003.
47. Quevedo J, Eguibar JR, Jimenez I, Schmidt RF, Rudomin P. Primary afferent depolarization of muscle afferents elicited by stimulation of joint afferents in cats with intact neuraxis and during reversible spinalization. J Neurophysiol 70: 1899-1910, 1993.
48. Roby-Brami A, Bussel B. Long-latency spinal reflex in man after flexor reflex afferent stimulation. Brain 110: 707-725, 1987.
49. Rossignol S, Frigon A. Recovery of locomotion after spinal cord injury: some facts and mechanisms. Annu Rev Neurosci 34: 413-440, 2011.
50. Rudomin P, Lomeli J, Quevedo J. Differential modulation of primary afferent depolarization of segmental and ascending intraspinal collaterals of single muscle afferents in the cat spinal cord. Exp Brain Res 156: 377-391, 2004a.
51. Rudomin P, Lomeli J, Quevedo J. Tonic differential supraspinal modulation of PAD and PAH of segmental and ascending intraspinal collaterals of single group I muscle afferents in the cat spinal cord. Exp Brain Res 159: 239-250, 2004b.
52. Rudomin P, Schmidt RF. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129: 1-37, 1999.
53. Schieppati M, Nardone A. Group II spindle afferent fibers in humans: their possible role in the reflex control of stance. Prog Brain Res 123: 461-472, 1999.
54. Sherrington CS. Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40: 28-121, 1910.
55. Stein RB, Kearney RE. Nonlinear behavior of muscle reflexes at the human ankle joint. J Neurophysiol 73: 65-72, 1995.
56. Valero-Cabre A, Fores J, Navarro X. Reorganization of reflex responses mediated by different afferent sensory fibers after spinal cord transection. J Neurophysiol 91: 2838-2848, 2004.
57. Vinay L, Jean-Xavier C. Plasticity of spinal cord locomotor networks and contribution of cation-chloride cotransporters. Brain Res Rev 57: 103-110, 2008.
58. Xia R, Rymer WZ. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord 43: 14-21, 2005.
59. Yang JF, Stein RB, James KB. Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans. Exp Brain Res 87: 679-687, 1991.